Indoor Exposure and Adverse Birth Outcomes Related to Fetal - MDPI

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Int. J. Environ. Res. Public Health 2014, 11, 5904-5933; doi:10.3390/ijerph110605904 OPEN ACCESS

International Journal of Environmental Research and Public Health ISSN 1660-4601 www.mdpi.com/journal/ijerph Review

Indoor Exposure and Adverse Birth Outcomes Related to Fetal Growth, Miscarriage and Prematurity—A Systematic Review Evridiki Patelarou 1,* and Frank J. Kelly 2 1

2

Florence Nightingale School of Nursing and Midwifery, King’s College London, London SE18WA, UK NIHR Environmental Hazards Health Protection Research Unit, MRC-PHE Centre for Environment and Health, King’s College London, London SE19NH, UK; E-Mail: [email protected]

* Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +44-207-848-3553 (ext. 3553). Received: 4 March 2014; in revised form: 19 May 2014 / Accepted: 21 May 2014 / Published: 3 June 2014

Abstract: The purpose of this review was to summarize existing epidemiological evidence of the association between quantitative estimates of indoor air pollution and all-day personal exposure with adverse birth outcomes including fetal growth, prematurity and miscarriage. We carried out a systematic literature search of MEDLINE and EMBASE databases with the aim of summarizing and evaluating the results of peer-reviewed epidemiological studies undertaken in “westernized” countries that have assessed indoor air pollution and all-day personal exposure with specific quantitative methods. This comprehensive literature search identified 16 independent studies which were deemed relevant for further review and two additional studies were added through searching the reference lists of all included studies. Two reviewers independently and critically appraised all eligible articles using the Critical Appraisal Skills Programme (CASP) tool. Of the 18 selected studies, 14 adopted a prospective cohort design, three were case-controls and one was a retrospective cohort study. In terms of pollutants of interest, seven studies assessed exposure to electro-magnetic fields, four studies assessed exposure to polycyclic aromatic hydrocarbons, four studies assessed PM2.5 exposure and three studies assessed benzene, phthalates and noise exposure respectively. Furthermore, 12 studies examined infant growth as the main birth outcome of interest, six examined spontaneous abortion and three studies assessed gestational age at birth and preterm delivery. This survey demonstrates that there is

Int. J. Environ. Res. Public Health 2014, 11 insufficient research on the possible association early life effects and that further research is needed.

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Keywords: pregnancy; gestational age; environmental exposures; environmental tobacco smoke; air pollution; indoor air pollution; birth weight; small for gestational age; fetal growth; preterm delivery

1. Introduction The root cause of many adverse birth outcomes is not well understood, although there is growing evidence that the environment can play an important role. The term “environment” is broad and may include nutrition, smoking and alcohol use, social networks, and air pollution both outdoor and indoor. The developing fetus is thought to be particularly susceptible to environmental pollutants and birth outcomes that may be influenced by exposure to environmental factors include gestational duration, infant growth, miscarriage/pregnancy loss and congenital anomalies [1]. A large body of evidence demonstrates that, in addition to parental smoking [2–4] and environmental tobacco smoke (ETS) [5], outdoor and indoor air pollutants may increase the risk of adverse birth outcomes, including low birth weight (LBW), premature births, and intrauterine growth retardation (IUGR) [1,6–8]. Several studies have associated maternal exposure to ambient air pollution (especially PM2.5) during pregnancy and a heightened risk of preterm delivery (PTD), low birth weight (LBW) and other adverse health effects [9]. In addition, a recent study with pooled data for 14 population-based mother-child cohort studies in 12 European countries confirmed previous findings that exposure to ambient air pollutants and traffic during pregnancy is associated with restricted fetal growth [10]. A number of studies conducted in developing countries have also addressed the effect of exposure to indoor air pollution (IAP) (mainly from solid fuel combustion processes) on diseases, such as respiratory infection, chronic obstructive pulmonary disease, cataract, asthma, heart diseases and adverse birth outcomes [11]. Pope et al. conducted meta-analyses to quantify the relation of indoor air pollution from solid fuel combustion processes with birth weight and stillbirth [12]. When women using solid fuel were compared with those using cleaner fuels it was found that solid fuel use was associated with increased risk of LBW and stillbirth (OR 1.38, 95% CI 1.25 to 1.52 and OR 1.51, 95% CI 1.23 to 1.85) [12]. A more recent review by Misra et al. aimed to establish a quantitative association between LBW attributable to IAP [11]. Seven studies were identified (six of them conducted in developing countries) and the meta-analysis indicated that the summary risk of LBW increased 1.45-fold due to IAP exposure [11]. Exposure to electromagnetic fields (EMF) in the indoor environment (home, work, social places) and its effect on pregnancy outcome still remains controversial and the majority of the published studies have focused on the potential effect of EMF on the risk of childhood leukemia [13–15]. These studies have showed relative risks slightly above 1.0 but most failed to assess personal exposure accurately instead using surrogates including wire code classification of the residence and retrospective spot measurements [14,16]. The effect of EMF on miscarriage/pregnancy loss has been studied only to a limited extent and examination has mostly been for exposure to video display

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terminals (VDT). In addition, the occurrence of adverse birth outcomes among women living or working in noisy environments has been also reported with some studies suggesting an association between noise exposure during pregnancy and low birth weight [17]. However, these studies had considerable limitations regarding exposure assessment as they did not manage to directly assess noise exposure and the possible periodic variation of noise exposure was not considered. Given that most people, especially pregnant women and children, spend most of their time indoors, the consequences of indoor exposure to environmental hazards range from negligible to severe, and can even be fatal to the unborn child in certain circumstances. Considering the scale of the problem and the potential severity of the associated risk our aim was to assess the effect of exposure to indoor environmental hazards on adverse birth outcomes among studies conducted in “westernized” countries. In this systematic review, exposures were assessed through quantitative measures among studies conducted in “westernized” countries on the development of adverse birth outcomes including infant growth, gestational age and miscarriage. 2. Methods 2.1. Literature Search Strategy A systematic review of the existing literature on indoor pollutants and adverse birth outcomes was carried out. We posed the following review question: “Given existing epidemiological evidence, what is the relationship between exposure of pregnant women to indoor pollutants and the risk of various adverse birth outcomes?” We drew up a review protocol in advance following standards outlined in the MOOSE Guidelines for Meta-Analyses and Systematic Reviews of Observational Studies [18]. Next we carried out a systematic, comprehensive bibliographic search using Medline (National Library of Medicine) database for the years 1946–March 2013, using the PubMed interface. Search terms used were chosen from the USNLM Institutes of Health list of Medical Subject Headings (MeSH) for 2013. These were: “Air Pollution, Indoor”; “Particulate Matter”; “Nicotine”; “Carbon Monoxide”; “Nitrogen Dioxide”; “Sulfur Dioxide”; “Polycyclic Hydrocarbons, Aromatic”; “Radon”; “Solvents”; “Asbestos”; “Ozone”; “Pesticides”; “Volatile Organic Compounds”; “Formaldehyde”; “Benzene”; “Toluene”; “Styrene”; “Dibutyl Phthalate”; “phthalate.mp.”; “Polyvinyl Chloride”; “Noise”; “Noise, Occupational”; “Electromagnetic Fields”; “Magnetic Fields”; “Pregnancy Outcome”; “Pre-Eclampsia”; “Pregnancy Outcome”; “Fetal Death”; “Premature Birth”; “Pregnancy Complications”; “Abortion, Spontaneous”; “Birth Weight”; “low birth weight.mp.”; “Infant, Low Birth Weight”; “Fetal Growth Retardation”; “Gestational Age”; “intrauterine growth.mp.”; “Embryonic and Fetal Development”; “Congenital Abnormalities”; “Hypertension, Pregnancy-Induced”; “Infant Mortality”; “Perinatal Mortality”; “Fetal Death”; “Infant, Premature”; and “preterm.mp.”. Full details of the search strategy and the key-words’ combination are provided in Table 1. The same search method was then repeated using the EMBASE database. Bibliographies of each retrieved study and reviews were also checked by hand for additional studies that met broad eligibility criteria.

Int. J. Environ. Res. Public Health 2014, 11 Table 1. Search terms used to identify relevant studies for the review. IAP § and Pregnancy Outcome Exposure 1. * Air Pollution, Indoor/ 2. * Particulate Matter/ 3. * Nicotine/ 4. * Carbon Monoxide/ 5. * Nitrogen Dioxide/ 6. * Sulfur Dioxide/ 7. * Polycyclic Hydrocarbons, Aromatic/ 8. * Radon/ 9. * Solvents/ 10. * Asbestos/ 11. * Ozone/ 12. * Pesticides/ 13. * Volatile Organic Compounds/ 14. * Formaldehyde/ 15. * Benzene/ 16. * Toluene/ 17. * Styrene/ 18. * Dibutyl Phthalate/or phthalate.mp. 19. * Polyvinyl Chloride/ 20. * Noise/or * Noise, Occupational/ 21. * Electromagnetic Fields/ 22. * Magnetic Fields/ 23. 1 or 2 or 3 or 4 or 5 or 6 or 7 or 8 or 9 or 10 or 11 or 12 or 13 or 14 or 15 or 16 or 17 or 18 or 19 or 20 or 21 or 22 Outcome 24. * Pregnancy Outcome 25. * Pre-Eclampsia/or * Pregnancy Outcome/or * Fetal Death/or * Premature Birth/or * Pregnancy Complications/or * Abortion, Spontaneous/ 26. * Birth Weight 27. low birth weight.mp. or * Infant, Low Birth Weight/ 28. Fetal Growth Retardation/or Gestational Age/or intrauterine growth.mp. or “Embryonic and Fetal Development”/ 29. * Congenital Abnormalities/ 30. * Hypertension, Pregnancy-Induced/ 31. * Infant Mortality/or *Perinatal Mortality/or *Fetal Death 32. * Infant, Premature/or preterm.mp. 33. 24 OR 25 OR 26 OR 27 OR 28 OR 29 OR 30 OR 31 OR 32 Combined terms 34. 23 AND 33 Note: § Abbreviation: IAP, indoor air pollution.

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2.2. Selection Criteria From the identified papers, studies meeting the following eligibility criteria were selected:    

papers published in peer-reviewed journal papers published in English language human epidemiological studies of any study design studies conducted in developed countries (definition was based on the list of Developing Countries provided by the International Statistical Institute)

Studies not meeting these criteria were excluded and studies meeting the criteria were shortlisted for inclusion in the review. The list was further narrowed down on the basis of their exposure assessment methods. Specifically, only studies characterising exposure with quantitative methods during pregnancy were included. We also decided to include studies that assessed all day exposure with the use of personal monitors given the fact that people and especially pregnant women, usually spend almost all (90%) of their time indoors (home, work, social places) [19–21]. 2.3. Literature Screening and Data Extraction Studies were evaluated for inclusion by two independent reviewers for relevance to the subject. Study selection was accomplished through four levels of study screening. Disagreement was resolved by discussion. At level 1 screening, studies were excluded by reviewing the title of the article. At level 2 screening, abstracts of all studies accepted at level 1 were reviewed for relevance. For level 3 screening, the full text was obtained for relevant papers and any citations for which a decision could not be made from the abstract- level 2. For level 4 screening, a hand search of recent reviews or already retrieved original articles was performed and additional referenced, manuscripts were included in the systematic review. Data were then extracted systematically from each selected study using a pre-designed standard data collection form. Information on study design, methods, pollutants and outcome of interest, source and timing of exposure, location of study, results and confounding factors used during statistical analyses were obtained. 2.4. Study Evaluation and Critical Appraisal of the Evidence Analyses of the data, as well as evaluation of the evidence presented in the articles, were performed with the use of the Critical Appraisal Skills Programme (CASP) in order to grade the evidence extracted [22,23]. The CASP tool uses a systematic approach to appraise three broad areas for consideration: study validity, an evaluation of methodological quality and presentation of results and an assessment of external validity [22,23]. There are 12 specific questions for cohort studies and 11 for case-control studies assessing the following: study validity, risk of bias in recruitment, exposure, outcome measurement, confounding factors, reporting of results and the transferability of findings. Each of the questions can be answered with “yes”, “no” or “can’t tell” and each study can have a maximum score of 12 (if cohort study) and 11 (if case-control study). In our review, two of the CASP questions were not included. The question, “Can the results be applied to the local population?” was not included because the focus of this review was not tied to a specific local population and

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the question, “Do the results of this study fit with other available evidence?” was not included for each individual study, as the purpose of this review was to compare results across studies. The articles were graded independently by the 2 reviewers who resolved any disagreements through consensus. The scores were used to grade the methodological quality of each study assessed (maximum score 10 for cohort and 9 for case-control studies). The grades given for each study rated the data related to this review article and may not reflect the overall quality of the study. 3. Results 3.1. Bibliographic Search Our combined search to MEDLINE and EMBASE retrieved 1,652 records. The initial screening of manuscript titles and abstracts excluded 1,604 records that did not meet the eligibility criteria. Common reasons for articles’ exclusion included studies conducted in developing countries, in non-English language and studies that did not develop a quantitative approach for assessing exposure. We excluded another 32 articles after examination of the full text. Additionally, two articles were retrieved by searching the reference lists of retrieved reviews and articles. Figure 1 shows the numbers of studies identified and selected/excluded in each phase of the search. Ultimately, eighteen articles were deemed suitable for inclusion in the review. Figure 1. Flow chart for selection of studies.

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3.2. Overview of the Included Studies Characteristics of the studies included in the analysis are given in Tables 2 and 3. Among the relevant studies three were case-control studies [24–26], one was a retrospective cohort study [27] and fourteen were prospective cohort studies [17,28–40]. Eight articles used data of studies conducted in USA [26–28,30,36–38,40], five in Poland [31–35], two in Finland [24,25], one in Taiwan [17], one in France [39] and one combined data from two prospective studies conducted in USA and in Poland [29]. Overall, among the retrieved studies exposure characterisation varied widely, particularly in terms of the exposure assessment methodology. Exposure assessment methods used in the studies are also described in Tables 2 and 3. In total, seven studies examined solely indoor exposure either at home [24,26,28] or at work [25,27] or at both places [36,37] and twelve studies referred to pregnancy cohort studies which assessed all day exposure to specific pollutants with the use of personal monitors [17,29–35,38–40]. In terms of the exposure of interest, seven studies investigated exposure to EMF [24–27,36,37], four articles exposure to fine particles smaller than 2.5 micrometers (PM2.5) [32–35], four polycyclic aromatic hydrocarbons (PAH) exposure [29–31,38], one to benzene exposure [39], one to phthalate exposure [40] and one to noise exposure [17]. Spontaneous abortion (SAB), pregnancy loss and miscarriage was the outcome of interest for five studies [24,25,27,36,37], infant growth was examined by eleven articles [17,28–35,38,39] and duration of gestation by three articles [29,30,40]. 3.3. Effects of Quantified Exposure to Indoor Pollutants on Birth Outcomes Seven studies were identified that addressed the potential effects of EMF or MF exposure and the risk of adverse birth outcome [24–28,36,37]. Below we present a short description of the methods and the main findings for each study (Table 4). The first study that measured EMF exposure and adverse birth outcomes was performed in 1991 [27]. Authors conducted a case-control study and performed specific EMF measurements of telephone operators who used VDT with a cohort of operators who did not use VDT. The aim of the study was to examine the association between SAB and the measured EMF at VDT workstations. No excess risk of SAB among women who were exposed to EMF during the first trimester of pregnancy (OR 0.93, 95% CI 0.63 to 1.38) was found. The following year, Lindbohm and colleagues conducted a study among women employed as bank clerks and clerical workers in three companies in Finland where specific measurement of the fields of the VDT were made [25]. The study showed that the OR for SAB for workers who had used a VDT with a high level of extremely low frequency MF (>0.9 μT) was 3.4 (95% CI 1.4–8.6) compared with workers using a terminal with a low level of MF (